Cycling of biogenic elements drives biogeochemical gold cycling

Abstract

Microorganisms are key-drivers of carbon-, nitrogen-, sulfur- and metal cycling on Earth. Through their metabolic activities they directly and indirectly link element cycles. This leads to the cycling of elements through the Earth’s ecosystems from/to the atmosphere to/from the lithosphere. Gold (Au) is a rare, redox-active, noble transition metal, which is neither essential as a nutrient nor, reputedly, mobile in the environment. Therefore, observations published in recent decades, which have shown that gold is highly mobile and subject to biogeochemical cycling largely driven by microbiota, have surprised many. Questions concerning the fundamental biogeochemical processes mediating gold cycling, the organisms involved and the benefits they may gain have puzzled researchers. In this review we integrate the cycling of the major biogenic elements carbon, nitrogen and sulfur with that of gold. We identify key-processes that drive gold cycling and evaluate how different chemical Au(I/III)-species affect microbiota that form biofilms on gold-bearing minerals and placer gold particles. Additionally, we assess how the cycling of the gold-associated metal(loid)s silver, copper, iron, manganese, mercury and arsenic is linked to that of gold. Microbially produced compounds resulting from carbon, nitrogen, sulfur, iron and manganese cycling (e.g., organic acids, cyanides, (thio)sulfates, ammonium, iron sulfides/oxy-hydroxides and managanese oxides) can each play important roles for the mobilization of gold. Highly toxic, mobile Au(I/III)-complexes affect the phylogenetic and functional composition of microbial communities resident on gold particles. This leads to gold detoxification coupled to active and passive biomineralization, and ultimately the aggregation and (trans)formation of metallic gold particles. The complex interplay between gold, microbiota and physicochemical conditions modified by these organisms (e.g., redox or pH) has throughout the Earth’s history led to the aggregation of gold particles (grains to nuggets), led to the formation of the largest known gold deposit (i.e., Witwatersrand paleo-placer), and the largest gold reservoir in seawater. Today it opens up exciting biotechnological pathways for mineral exploration, processing and remediation.